Chapter 4 C4 Photosynthesis: Kranz Forms and Single-Cell C4 in Terrestrial Plants

Edwards, Gerald E.; Voznesenskaya, Elena V.

doi:10.1007/978-90-481-9407-0_4

Cited by 90 publications

(175 citation statements)

References 120 publications

Supporting

Mentioning

163

Contrasting

Unclassified

Order By: Relevance

“…However, over the next 20-30 Myr, the C 4 pathway continued to evolve in other lineages, suggesting that low CO 2 concentrations acted as a preconditioning event rather than the sole trigger for C 4 evolution [16]. Other factors such as high temperatures, salinity and fire frequency in tropical and subtropical regions have been proposed to contribute to the polyphyletic evolution of C 4 photosynthesis [24].…”

Section: The Biochemistry and Evolution Of C 4 Photosynthesismentioning

confidence: 99%

Recruitment of pre-existing networks during the evolution of C ₄ photosynthesis

Reyna-Llorens¹,

Hibberd²

2017

Phil. Trans. R. Soc. B

View full text Add to dashboard Cite

During C 4 photosynthesis, CO 2 is concentrated around the enzyme RuBisCO. The net effect is to reduce photorespiration while increasing water and nitrogen use efficiencies. Species that use C 4 photosynthesis have evolved independently from their C 3 ancestors on more than 60 occasions. Along with mimicry and the camera-like eye, the C 4 pathway therefore represents a remarkable example of the repeated evolution of a highly complex trait. In this review, we provide evidence that the polyphyletic evolution of C 4 photosynthesis is built upon pre-existing metabolic and genetic networks. For example, cells around veins of C 3 species show similarities to those of the C 4 bundle sheath in terms of C 4 acid decarboxylase activity and also the photosynthetic electron transport chain. Enzymes of C 4 photosynthesis function together in gluconeogenesis during early seedling growth of C 3 Arabidopsis thaliana. Furthermore, multiple C 4 genes appear to be under control of both light and chloroplast signals in the ancestral C 3 state. We, therefore, hypothesize that relatively minor rewiring of pre-existing genetic and metabolic networks has facilitated the recurrent evolution of this trait. Understanding how these changes are likely to have occurred could inform attempts to install C 4 traits into C 3 crops.This article is part of the themed issue 'Enhancing photosynthesis in crop plants: targets for improvement'.

show abstract

Section: The Biochemistry and Evolution Of C 4 Photosynthesismentioning

confidence: 99%

Recruitment of pre-existing networks during the evolution of C ₄ photosynthesis

Reyna-Llorens¹,

Hibberd²

2017

Phil. Trans. R. Soc. B

View full text Add to dashboard Cite

show abstract

“…6). In C 4 photosynthesis, there is cooperation between the two compartments and their respective chloroplast types in capturing atmospheric CO 2 and donating it to the C 3 cycle and in providing the assimilatory power needed for C 4 photosynthesis (Edwards and Walker, 1983;Edwards and Voznesenskaya, 2011). In NAD-ME-type C 4 species, the minimum energy requirement to support an Asp-Ala-type C 4 cycle is two ATP per CO 2 delivered and three ATP and two NADPH per CO 2 assimilated in the C 3 cycle.…”

Section: Distribution Of Chloroplasts Between the Two Domainsmentioning

confidence: 99%

Resolving the Compartmentation and Function of C4 Photosynthesis in the Single-Cell C4 Species Bienertia sinuspersici

2011

Self Cite

View full text Add to dashboard Cite

Bienertia sinuspersici is a land plant known to perform C 4 photosynthesis through the location of dimorphic chloroplasts in separate cytoplasmic domains within a single photosynthetic cell. A protocol was developed with isolated protoplasts to obtain peripheral chloroplasts (P-CP), a central compartment (CC), and chloroplasts from the CC (C-CP) to study the subcellular localization of photosynthetic functions. Analyses of these preparations established intracellular compartmentation of processes to support a NAD-malic enzyme (ME)-type C 4 cycle. Western-blot analyses indicated that the CC has Rubisco from the C 3 cycle, the C 4 decarboxylase NAD-ME, a mitochondrial isoform of aspartate aminotransferase, and photorespiratory markers, while the C-CP and P-CP have high levels of Rubisco and pyruvate, Pidikinase, respectively. Other enzymes for supporting a NAD-ME cycle via an aspartate-alanine shuttle, carbonic anhydrase, phosophoenolpyruvate carboxylase, alanine, and an isoform of aspartate aminotransferase are localized in the cytosol. Functional characterization by photosynthetic oxygen evolution revealed that only the C-CP have a fully operational C 3 cycle, while both chloroplast types have the capacity to photoreduce 3-phosphoglycerate. The P-CP were enriched in a putative pyruvate transporter and showed light-dependent conversion of pyruvate to phosphoenolpyruvate. There is a larger investment in chloroplasts in the central domain than in the peripheral domain (6-fold more chloroplasts and 4-fold more chlorophyll). The implications of this uneven distribution for the energetics of the C 4 and C 3 cycles are discussed. The results indicate that peripheral and central compartment chloroplasts in the single-cell C 4 species B. sinuspersici function analogous to mesophyll and bundle sheath chloroplasts of Kranz-type C 4 species.Rubisco is the central CO 2 fixation enzyme in plants. It is a bifunctional enzyme, catalyzing the carboxylation as well as the oxygenation of ribulose-bisphosphate (RuBP) to 3-phosphoglycerate (3-PGA) and phosphoglycolate, respectively. While 3-PGA is subsequently utilized in the C 3 cycle to produce triose-phosphates, phosphoglycolate has no known metabolic use (Ogren, 1984) and needs to be detoxified by the plant. This process is known as photorespiration, which is not only energy consuming but also results in a net loss of previously fixed carbon and nitrogen. The rate of carboxylation versus oxygenation through Rubisco is directly related to the availability of CO 2 and the concentration of oxygen competing for the catalytic site of the enzyme. Since Rubisco is thought to have evolved under much higher levels of CO 2 than current atmospheric concentrations, it is believed that photorespiration was insignificant earlier in photosynthetic organisms. Under current atmospheric CO 2 levels, however, significant amounts (e.g. up to 25%) of previously fixed carbon may be lost through RuBP oxygenase activity under conditions that favor photorespiration, like high temperatures or water stres...

show abstract

“…Although several examples of C 4 photosynthesis operating in single cells have been described (Reiskind et al, 1997;Casati et al, 2000;Reinfelder et al, 2000;Voznesenskaya et al, 2002Voznesenskaya et al, , 2003, most C 4 species compartmentalize carboxylation and decarboxylation activities into two distinct cell types. At least 22 variations of two-celled "Kranz" anatomy have been documented (Dengler and Nelson, 1999;Edwards and Voznesenskaya, 2011;Sage et al, 2012) whereby different cell types have been coopted as the photosynthetic carbon assimilation and photosynthetic carbon reduction tissue. In the grasses, nine types of Kranz anatomy have been described (Edwards and Voznesenskaya, 2011).…”

mentioning

confidence: 99%

“…At least 22 variations of two-celled "Kranz" anatomy have been documented (Dengler and Nelson, 1999;Edwards and Voznesenskaya, 2011;Sage et al, 2012) whereby different cell types have been coopted as the photosynthetic carbon assimilation and photosynthetic carbon reduction tissue. In the grasses, nine types of Kranz anatomy have been described (Edwards and Voznesenskaya, 2011). Five of these nine types have two sheaths that surround each vascular bundle.…”

mentioning

confidence: 99%

Individual Maize Chromosomes in the C3 Plant Oat Can Increase Bundle Sheath Cell Size and Vein Density

et al. 2012

View full text Add to dashboard Cite

C4 photosynthesis has evolved in at least 66 lineages within the angiosperms and involves alterations to the biochemistry, cell biology, and development of leaves. The characteristic “Kranz” anatomy of most C4 leaves was discovered in the 1890s, but the genetic basis of these traits remains poorly defined. Oat × maize addition lines allow the effects of individual maize (Zea mays; C4) chromosomes to be investigated in an oat (Avena sativa; C3) genetic background. Here, we have determined the extent to which maize chromosomes can introduce C4 characteristics into oat and have associated any C4-like changes with specific maize chromosomes. While there is no indication of a simultaneous change to C4 biochemistry, leaf anatomy, and ultrastructure in any of the oat × maize addition lines, the C3 oat leaf can be modified at multiple levels. Maize genes encoding phosphoenolpyruvate carboxylase, pyruvate, orthophosphate dikinase, and the 2′-oxoglutarate/malate transporter are expressed in oat and generate transcripts of the correct size. Three maize chromosomes independently cause increases in vein density, and maize chromosome 3 results in larger bundle sheath cells with increased cell wall lipid deposition in oat leaves. These data provide proof of principle that aspects of C4 biology could be integrated into leaves of C3 crops.

show abstract

Chapter 4 C4 Photosynthesis: Kranz Forms and Single-Cell C4 in Terrestrial Plants

Cited by 90 publications

References 120 publications

Recruitment of pre-existing networks during the evolution of C ₄ photosynthesis

Recruitment of pre-existing networks during the evolution of C ₄ photosynthesis

Resolving the Compartmentation and Function of C4 Photosynthesis in the Single-Cell C4 Species Bienertia sinuspersici

Individual Maize Chromosomes in the C3 Plant Oat Can Increase Bundle Sheath Cell Size and Vein Density

Contact Info

Product

Resources

About

Chapter 4 C4 Photosynthesis: Kranz Forms and Single-Cell C4 in Terrestrial Plants

Cited by 90 publications

References 120 publications

Recruitment of pre-existing networks during the evolution of C 4 photosynthesis

Recruitment of pre-existing networks during the evolution of C 4 photosynthesis

Resolving the Compartmentation and Function of C4 Photosynthesis in the Single-Cell C4 Species Bienertia sinuspersici

Individual Maize Chromosomes in the C3 Plant Oat Can Increase Bundle Sheath Cell Size and Vein Density

Contact Info

Product

Resources

About

Recruitment of pre-existing networks during the evolution of C ₄ photosynthesis

Recruitment of pre-existing networks during the evolution of C ₄ photosynthesis